Response to interferons and antibacterial innate immunity in the absence of tyrosine-phosphorylated STAT1

EMBO Rep. 2016 Mar;17(3):367-82. doi: 10.15252/embr.201540726. Epub 2016 Feb 12.

Abstract

Signal transducer and activator of transcription 1 (STAT1) plays a pivotal role in the innate immune system by directing the transcriptional response to interferons (IFNs). STAT1 is activated by Janus kinase (JAK)-mediated phosphorylation of Y701. To determine whether STAT1 contributes to cellular responses without this phosphorylation event, we generated mice with Y701 mutated to a phenylalanine (Stat1(Y701F)). We show that heterozygous mice do not exhibit a dominant-negative phenotype. Homozygous Stat1(Y701F) mice show a profound reduction in Stat1 expression, highlighting an important role for basal IFN-dependent signaling. The rapid transcriptional response to type I IFN (IFN-I) and type II IFN (IFNγ) was absent in Stat1(Y701F) cells. Intriguingly, STAT1Y701F suppresses the delayed expression of IFN-I-stimulated genes (ISG) observed in Stat1(-/-) cells, mediated by the STAT2/IRF9 complex. Thus, Stat1(Y701F) macrophages are more susceptible to Legionella pneumophila infection than Stat1(-/-) macrophages. Listeria monocytogenes grew less robustly in Stat1(Y701F) macrophages and mice compared to Stat1(-/-) counterparts, but STAT1Y701F is not sufficient to rescue the animals. Our studies are consistent with a potential contribution of Y701-unphosphorylated STAT1 to innate antibacterial immunity.

Keywords: STAT1; innate immunity; interferon; pathogen; phosphorylation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Cells, Cultured
  • Immunity, Innate*
  • Interferon-Stimulated Gene Factor 3, gamma Subunit / metabolism
  • Interferons / metabolism*
  • Legionnaires' Disease / immunology*
  • Listeriosis / immunology*
  • Macrophages / immunology
  • Mice
  • Mice, Inbred C57BL
  • Mutation, Missense
  • Phosphorylation
  • Protein Processing, Post-Translational*
  • STAT1 Transcription Factor / deficiency*
  • STAT1 Transcription Factor / genetics
  • STAT1 Transcription Factor / metabolism
  • STAT2 Transcription Factor / metabolism
  • Second Messenger Systems

Substances

  • IRF9 protein, mouse
  • Interferon-Stimulated Gene Factor 3, gamma Subunit
  • STAT1 Transcription Factor
  • STAT2 Transcription Factor
  • Stat1 protein, mouse
  • Stat2 protein, mouse
  • Interferons